Two Feathered Dinosaurs from Northeastern China

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Two feathered dinosaurs from northeastern China

Ji Qiang*, Philip J. Currie†, Mark A. Norell‡ & Ji Shu-An* 8 * National Geological Museum of China, Yangrou Hutong 15, Xisi, 100034 Beijing, People’s Republic of China † Royal Tyrrell Museum of Palaeontology, Box 7500, Drumheller, Alberta T0J 0Y0, Canada ‡ American Museum of Natural History, Central Park West at 79th Street, New York, New York 10024-5192, USA

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Current controversy over the origin and early evolution of birds centres on whether or not they are derived from coelurosaurian theropod dinosaurs. Here we describe two theropods from the Upper Jurassic/Lower Cretaceous Chaomidianzi Formation of Liaoning province, China. Although both theropods have feathers, it is likely that neither was able to ﬂy. Phylogenetic analysis indicates that they are both more primitive than the earliest known avialan (bird), Archaeopteryx. These new fossils represent stages in the evolution of birds from feathered, ground-living, bipedal dinosaurs.

Dinosauria Owen 1842 There are two thin, flat, featureless sternal plates. The clavicles are Theropoda Marsh 1881 fused into a broad, U-shaped furcula (interclavicular angle is about Maniraptora Gauthier 1986 60Њ)asinArchaeopteryx, Confuciusornis and many non-avian Unnamed clade theropods. The forelimb is shorter than the hindlimb. The arm is Protarchaeopteryx robusta Ji & Ji 1997 shorter (compared to the femur) than it is in birds, but is longer than those of long-armed non-avian coelurosaurs such as Holotype. National Geological Museum of China, NGMC 2125 dromaeosaurids and oviraptorids (Table 2). The better preserved (Figs 1, 2 and 3). right wrist of NGMC 2125 has a single semilunate carpal capping Locality and horizon. Sihetun area near Beipiao City, Liaoning, the first two metacarpals. The hand has the normal theropod China. Jiulongsong Member of Chaomidianzi Formation, Jehol phalangeal formula of 2-3-4-x-x. The manus is longer than either Group1. This underlies the Yixian Formation, the age of which the humerus or radius. Compared to femur length, the hand is more has been determined to be Late Jurassic to Early Cretaceous3,4. elongate than those of any theropods other than Archaeopteryx9 and Diagnosis. Large straight premaxillary teeth, and short, bulbous Confuciusornis (Table 2). More advanced birds such as Cathayornis maxillary and dentary teeth, all of which are primitively serrated. have shorter hands10. Phalanges III-1 and III-2 in the hand of Rectrices form a fan at the end of the tail. Protarchaeopteryx are almost the same size, and are about half the Description. The skull of Protarchaeopteryx is shorter than the length of III-3. The unguals are long and sharp, and keratinous femur (Table 1). There are four serrated premaxillary teeth (Fig. 1c), sheaths are preserved on two of them. with crown heights of up to 12 mm. Premaxillary teeth of The preacetabular blade of the ilium is about the same length as coelophysids5, compsognathids6,7 and early birds lack serrations, the postacetabular blade. The pubic boot expands posteriorly. but premaxillary denticles are present in most other theropods. Six Anteriorly, the pubis is not exposed. maxillary and seven dentary teeth are preserved (Fig. 1), all of which The tibia is longer than the femur, as it is in most advanced are less than a quarter the height of the premaxillary teeth. They theropods and early birds. It is not known if the fibula extended to most closely resemble those of Archaeopteryx8 in shape (Figs 1b, c the tarsus. and 2b, c), but have anterior and posterior serrations (7–10 The metatarsals are separate from each other and the distal serrations per mm). tarsals. Metatarsal I is centred halfway up the posteromedial edge The amphicoelous posterior cervicals are the same length as the of the second metatarsal. In perching birds such as Sinornis9, posterior dorsals, which have large pleurocoels. If the lengths of metatarsal I is positioned near the end of metatarsal II and is missing segments of the tail are accounted for, there were fewer than retroverted. Its condition in Archaeopteryx is intermediate. Pedal 28 caudals. Vertebrae increase in length from proximal to mid- unguals are smaller than manual unguals. caudals, as in most non-avian coelurosaurs. A clump of at least six plumulaceous feathers is preserved anterior

Table 1 Lengths of elements in Protarchaeopteryx and Caudipteryx Table 2 Relative proportions of elements in relevant avian and non-avian theropods Element NGMC 2125 NGMC 97-4-A NGMC 97-9-A ...... Element Drom Ov Tro Cx Px Ax Con Body length 690 890 725 ...... Skull 70 76 79 Arm/F 1.8–2.6 1.5–1.8 1.8 1.5 2.4 3.7 3.9 Sternal plates 25 36 — S/H 0.8 1.0–1.2 — 1.1 — 0.6 0.8 Humerus 88 69 70 R/H 0.7–0.8 0.8–0.9 0.6–0.7 0.9 0.8 0.9 0.8 Arm (humerus to end of phalange II-2) 297 214 220 Manus/H 0.9–1.2 1.2–1.4 1.3 1.2 1.6 1.2 1.3 Ilium 95 101 — Manus/F 1.0 0.7–1.0 0.8 0.6 1.2 1.5 1.6 Ischium — 77 — McI/McII 0.4–0.5 0.4–0.6 0.3 0.4 0.4 0.3 0.4 Leg (femur to end of phalange III-4) 450 550 540 T/F 1.1–1.4 1.2 1.1–1.2 1.2 1.3 1.4 1.1 Femur 122 147 149 Leg/F 3.6 3.3 3.8 3.7 3.7 3.8 3.3 Tibia 160 188 182 Leg/arm 1.4 1.7 2.1 2.5 1.5 1.1 0.8 Tibia 160 188 182 ...... Metatarsal III 85 115 117 All data were collected from original specimens by P.J.C. Ax, Archaeopteryx; Con, ...... Confuciusornis; Cx, Caudipteryx; Drom, dromaeosaurids; F, femur; H, humerus; L, length; Length measurements are given in millimetres. NGMC 2125, Protarchaeopteryx; NGMC Mc, metacarpal; Ov, oviraptorids; Px, Protarchaeopteryx; R, radius; S, scapula; T, tibia; Tro, 97.4-A and NGMC 97-9-A, Caudipteryx. troodontids.

Nature © Macmillan Publishers Ltd 1998 NATURE | VOL 393 | 25 JUNE 1998 753 articles to the chest, with some showing well-developed vanes (Fig. 3a). Jiahua, vice-premier of China and an avid supporter of the scientiﬁc Evenly distributed plumulaceous feathers up to 27 mm long are work in Liaoning. associated with ten proximal caudal vertebrae. Twenty-millimetre Holotype. NGMC 97-4-A (Figs 4 and 5b). plumulaceous feathers are preserved along the lateral side of the Paratype. NGMC 97-9-A (Fig. 5d). right femur and the proximal end of the left femur. Locality and horizon. Sihetun area, Liaoning. Jiulongsong Member Parts of more than twelve rectrices are preserved11 attached to the of the Chaomidianzi Formation. distal caudals. One of the symmetrical tail feathers (Fig. 3b) extends Diagnosis. Elongate, hooked premaxillary teeth with broad roots; 132 mm from the closest tail vertebra, and has a long tapering rachis maxilla and dentary edentulous. Tail short (one-quarter of the with a basal diameter of 1.5 mm. The well-formed pennaceous vanes length of the body). Arm is long for a non-avian theropod; short of Protarchaeopteryx show that barbules were present. The vane is manual claws. Leg-to-arm ratio, 2.5. 8 5.3 mm wide on either side of the rachis. At midshaft, ﬁve barbs come Description. The skulls of both specimens of Caudipteryx are off the rachis every 5 mm (compared with six in Archaeopteryx), and shorter than the corresponding femora because of a reduction in individual barbs are 15 mm long. As in modern rectrices, the barbs the length of the antorbital region. The relatively large premaxilla at the base of the feather are plumulaceous. (Figs 6 and 7) borders most of the large external naris. The maxilla and nasal are short, but the frontals and jugals are long. The lacrimal Maniraptora Gauthier 1986 of NGMC 97-4-A is an inverted L-shaped, pneumatic bone. Scleral Unnamed clade plates are preserved in the 20-mm-diameter orbits of both speci- Diagnosis. The derived presence of a short tail (less than 23 caudal mens. The tall quadratojugal seems to have contacted the squamosal vertebrae) and arms with remiges attached to the second digit. and abutted the lateral surface of the quadrate. The single-headed quadrate is vertical in orientation. The ectopterygoid has a normal Caudipteryx zoui gen. et sp. nov. theropod hooklike jugal process. There is a broad, beak-like margin at the symphysis of the dentaries. Posteriorly, the dentary bifurcates Etymology. ‘Caudipteryx’ means ‘tail feather’, ‘zoui’: refers to Zou around a large external mandibular fenestra as in oviraptorids. A

Nature © Macmillan Publishers Ltd 1998 754 NATURE | VOL 393 | 25 JUNE 1998 articles

R Figure 2 Protarchaeopteryx robusta. a, Outline of the specimen shown in Fig.1a. b, Outline of the left dentary teeth shown in Fig.1b. c, Drawing of the front of the jaws, showing the large size of the premaxillary teeth compared with maxillary and dentary ones. Abbreviations: Co, coracoid; d, dentary; F, femur; f, feathers; Fib, ﬁbula; Fu, furcula; H, humerus; m, maxilla; P, pubis; pm, premaxilla; R, radius; S, scapula; St, sternal plate; T, tibia; U, ulna. Numbers represent tooth positions from front to back.

Figure 1 Protarchaeopteryx robusta. a (facing page), NGMC 2125, holotype. Scale bar, 5 cm. b, Fourth to sixth left dentary teeth. Scale bar,1 mm. c, Premaxillaryteeth showing small serrations. Scale bar, 5 mm.

Nature © Macmillan Publishers Ltd 1998 NATURE | VOL 393 | 25 JUNE 1998 755 articles well-developed, sliding intramandibular joint is present between Each segment of gastralia is formed by two pairs of slender, dentary and surangular. tapering rods, as in all non-avian theropods, Protarchaeopteryx and There are four teeth in each premaxilla. They have elongate, early birds8,9,13,14. needlelike crowns, and the roots are five times wider than the The paired sternals are similar to those of dromaeosaurids and crowns (Fig. 7b). The lingual wall of the root of the third right tooth oviraptorids. Confuciusornis had a relatively larger, unkeeled ster- has been resorbed for the crown of a replacement tooth. The teeth num. Some short bones with slight expansions at each end are seem to have been procumbent, with an inflection at the gumline. found near the sternal plates of NGMC 97-9-A, and may be sternal Caudipteryx had no maxillary or dentary teeth. ribs. There are ten amphicoelous cervical vertebrae and five sacrals as The scapula is longer than the humerus, whereas the scapula-to- in most non-avian theropods and Archaeopteryx8,12. The tail of humerus ratio is less than 1.0 in flying birds (Table 2) because of 8 NGMC 97-4-A is articulated and well-preserved, and includes 22 humerus elongation. The clavicles are fused into a broad, U-shaped vertebrae, as in Archaeopteryx. It is shorter than the 30-segment tails furcula in NGMC 97-9-A as in Archaeopteryx, Confuciusornis and of oviraptorids. Most other non-avian theropods have much longer many non-avian theropods. tails. Caudals do not become longer posteriorly, as they do in most Compared to the humerus, forearm length is similar to that in non-avian theropods and Archaeopteryx. Almost two-thirds of the oviraptorosaurs (Table 2), Archaeopteryx and Protarchaeopteryx. In tail of NGMC 97-4-A is preserved as a straight rod, but the vertebrae more advanced birds15,16, the radius is longer than the humerus. The are not fused. The first six haemal spines are elongate, rodlike external surface of the ulna, as in Archaeopteryx8, lacks any evidence structures. More posterior haemal spines decrease in height, but of quill nodes. expand anteriorly and posteriorly (Fig. 5a). There are three carpals preserved in NGMC 97-4-A, including a large semi-lunate one that caps metacarpals I and II as in dromaeosaurids, oviraptorids, troodontids, Archaeopteryx, Confuciusornis and other birds. Four carpals have been recognized in Archaeopteryx12. A large triangular radiale sits between the semi- lunate and the radius. A small carpal articulates with the third metacarpal. A thin wedge of bone at the end of the ulna is probably a fragment of gastralia. The unfused metacarpals and digits of both specimens are well preserved. The third metacarpal is almost as long as the second, but is more slender. The hand has the normal theropod phalangeal

Figure 3 Protarchaeopteryx robusta, NGMC 2125. a, Contour and plumulaceous feathers. Scale bar,10 mm. b, Rectrices. Scale bar, 5 mm.

Nature © Macmillan Publishers Ltd 1998 756 NATURE | VOL 393 | 25 JUNE 1998 articles formula of 2-3-4-x-x. The manus is longer than either the humerus acetabular region than that of Protarchaeopteryx, and closely or the radius, which is a primitive characteristic shared with most resembles the ilium of dromaeosaurids18. The tapering post- non-avian coelurosaurs, Archaeopteryx9 and Confuciusornis. In acetabular region is lower and longer than the preacetabular. The contrast with Archaeopteryx, Confuciusornis, Protarchaeopteryx pubic penduncle is anteroposteriorly elongated, and has a notch and many non-avian theropods (ornithomimids, troodontids, (Figs 4 and 5b) in the ventral margin that divides the suture into two dromaeosaurids and oviraptorids), the manus is relatively short surfaces. This notch and the deep pubic peduncle of the ischium are compared with the femur. characteristic of opisthopubic pelves. The ischium has no dorsal The curved second manual ungual is about two-thirds the size of process such as that found in Archaeopteryx and Confuciusornis, and the same element in Protarchaeopteryx, and is less than 70% the the shaft curves down and back. A well-developed ventromedial length of the penultimate phalanx. ﬂange is present, perhaps indicating contact between elements. In8 Pelvic elements are unfused, as they are in all non-avian ther- general appearance, the ischium most closely resembles those of opods (except some ceratosaurs) and the most primitive birds16. non-avian coelurosaurs. The acetabulum is large, comprising almost a quarter of the length The ratio of hindlimb-to-forelimb length is higher than in other of the ilium (the ratio of acetabulum-to-ilium length is less than coelurosaurs (Table 2) except alvarezsaurids19, which had excep- 0.11 in birds17). It has a deeper, shorter, more squared-off pre- tionally short arms. The greater trochanter is separated from the

Figure 6 Caudipteryx zoui, skull of NGMC 97-9-A in right lateral view. Scale bar,1 cm.

Figure 7 Caudipteryx zou. a, Sketch of skull shown in Fig. 6. b, Premaxillary tooth lacrymal; m, maxilla; n, nasal; ns, neural spine; p, parietal; pm, premaxilla; po, of NGMC 97-4-A, showing resorption pit and germ tooth. Abbreviations: an, postorbital; q, quadrate; qj, quadratojugal; sa, surangular; sp, scleral plate; spl, angular; d, dentary; ec, ectopterygoid; eo, exoccipital; f, frontal; h, hyoid; j, jugal; l, splenial; t, premaxillary teeth.

Nature © Macmillan Publishers Ltd 1998 NATURE | VOL 393 | 25 JUNE 1998 757 articles lesser trochanter of the femur by a shallow notch, and forms a phalanx II-1, and the base of phalanx II-2 of NGMC 97-4-A raised, semi-lunate rim that is similar to the trochanter femoris of (Fig. 8a). Each remex has a well-preserved rachis and vane. The birds, troodontids and avimimids. most distal remex is less than 30 mm long. The second most distal None of the fibulae is complete, but NGMC 97-9-A has a socket remex is 63.5 mm long, is symmetrical, and has 6.5-mm-long barbs for the distal end of the fibula formed by the calcaneum, astragalus on either side of the rachis. The fourth most distal primary remex is and tibia. The astragalus is not fused to the tibia. The ascending 95 mm long and is longer than the humerus. Unfortunately, the process of NGMC 97-9-A (Fig. 5e) extends 22% of the distance up distal ends of the remaining remiges are not preserved. In flying the front surface of the tibia, compared with 12% in Archaeopteryx12. birds (even Archaeopteryx12), each remex is longer than they are in As in Archaeopteryx8, Confuciusornis10 and most non-avian thero- Caudipteryx, and the most distal remiges are the longest. For pods, the calcaneum is retained as a separate, disk-like element. Two example, the remiges of Archaeopteryx22 are more than double the 8 distal tarsals are positioned over the third and fourth metatarsals, as length of the femur. The barbs on either side of the rachis are in Archaeopteryx, Buluochia20 and all non-avian theropods that lack symmetrical, contrasting with Archaeopteryx and modern flying fused tarsometatarsals. birds23. The metatarsals of Caudipteryx are not fused; this is the plesio- The holotype preserves ten complete and two partial rectrices. morphic condition expressed in most non-avian theropods. Meta- Eleven are attached to the left side of the tail, and were probably tarsal I is centred about a quarter of the way up the posteromedial paired with another eleven feathers on the right side (only the corner of the second metatarsal. The third is the longest of the terminal feather is preserved). Two rectrices are attached to each side metatarsals, and in anterior view completely separates the second of the last five or six caudal vertebrae, but not to more anterior ones. and fourth metatarsals, unlike in the arctometatarsalian condition NGMC 97-9-A preserves most of nine retrices. In Archaeopteryx, of many theropods21. Nevertheless, at midshaft the third metatarsal rectrices are associated with all but the first five or six caudals12,22. is thin anteroposteriorly and is triangular in cross-section. The Each rachis has a basal diameter of 0.74 mm and tapers distally. All pedal unguals are triangular in cross-section and are about the same the feathers appear to be symmetrical (Fig. 8b), although in most size as the manual unguals. cases the tips of the barbs of adjacent feathers overlap. The vane of At least fourteen remiges are attached to the second metacarpal, the sixth feather is 6 mm wide on either side of the rachis.

Figure 4 Caudipteryx zoui, holotype, NGMC 97-4-A. Scale bar, 5 cm.

The body of NGMC 97-4-A, especially the hips and the base of the ambiguous ones (characters 4, 5, 10, 11, 15, 19, 24, 37, 85 and 86). tail, is covered by small, plumulaceous feathers of up to 14 mm long. Caudipteryx is separated from the Avialae by three unambiguous Both specimens have concentrations of small polished and characters (7, 8 and 71) and additional ambiguous ones (characters rounded pebbles in the stomach region. These gastroliths are up 5, 6, 9, 10, 11, 18, 24, 39, 40, 56 and 69). The important characteristic to 4.5 mm in diameter, although most are considerably less than of this phylogeny is that the Avialae (not including 4 mm wide. Protarchaeopteryx and Caudipteryx) is monophyletic; this placement is supported by the unequivocal presence of a quadratojugal Phylogenetic analysis that is joined to the quadrate by a ligament17 (character 7), the We examined the systematic positions of Protarchaeopteryx and absence of a quadratojugal squamosal contact (character 8) and a Caudipteryx by coding these specimens for the 90 characters used in reduced or absent process of the ischium (character 71). 8 an analysis of avialan phylogeny24 (for a matrix of these characters, As characters dealing with feathers cannot be scored relative to see Supplementary Information). Characters were unordered, and a outgroup conditions, they were not used in the phylogenetic tree was produced using the branch-and-bound option of PAUP25. analysis. However, our analysis indicates that feathers can no We rooted the tree with Velociraptorinae26,27. A single tree resulted longer be used in the diagnosis of the Avialae. with a length of 110 steps, a retention index of 0.849 and a consistency index of 0.855. Analysis shows Caudipteryx to be the Discussion sister group to the Avialae, and Protarchaeopteryx to be unresolved The three Protarchaeopteryx and Caudipteryx individuals were close from the Velociraptorinae root (Fig. 9). The placement of to maturity at the time of death. The neural spines seem to be fused Protarchaeopteryx as the sister group to Caudipteryx + Avialae, as to cervical and dorsal centra in Protarchaeopteryx. Sternal plates the sister group to Velociraptorinae, or as the sister group to ossify late in the ontogeny of non-avian theropods, and are present Velociraptorinae + (Caudipteryx + Avialae) are equally well sup- in both Caudipteryx and Protarchaeopteryx. Well-ossified sternal ported by the data. Characters that define the Caudipteryx + Avialae ribs, wrist bones and ankle bones in Caudipteryx also indicate the clade in the shortest tree include unambiguous (uninfluenced by maturity of the specimens. missing data or optimization) characters 2 and 12 and several more The remiges of Caudipteryx and the rectrices of both

Figure 5 Caudipteryx zoui. a, Haemal spines from the fourth, sixth, eighth, tions: a, astragalus; c, calcaneum; Co, coracoid; F, femur; g, gastroliths; H, eleventh and thirteenth caudal vertebrae (from left to right) of NGMC 97-4-A in left humerus; I, ilium; Is, ischium; P, pubis; R, radius; S, scapula; St, sternal plate; T, lateral view. b, Drawing of the specimen shown in Fig. 4a. c, Wrist of NGMC 97-4- tibia; U, ulna;?, possibly fragment of gastralia. Roman numerals represent digit A. d, Drawing of NGMC 97-9-A. e, Proximal tarsals of NGMC 97-9-A. Abbrevia- numbers.

Figure 8 Feathers of Caudipteryx zoui, NGMC 97-4-A. a, Remiges of left arm. Scale bar,1.75 cm. b, Rectrices, showing colour banding. Scale bar,1 cm.

Protarchaeopteryx and Caudipteryx have symmetrical veins, whereas ones. It seems unlikely that this animal was capable of active flight. even those of Archaeopteryx are asymmetrical. Birds with asymme- The relatively long legs of Protarchaeopteryx and Caudipteryx, both trical feathers are generally considered to be capable of flight23, but it of which have the hallux positioned high and orientated antero- is possible that an animal with symmetrical feathers could also fly. medially, indicate that they were ground-dwelling runners. Relative arm length of Protarchaeopteryx is shorter than that of Paired rectrices of Protarchaeopteryx and Caudipteryx are Archaeopteryx, but is longer than in non-avian coelurosaurs. The restricted to the end of the tail, whereas in Archaeopteryx they arms of Caudipteryx, in contrast, are shorter than those of most extend over more than two-thirds the length of the tail12. Wherever non-avian coelurosaurs; the remiges are only slightly longer than preservation made it possible, we found semi-plumes and down- the humerus; and the distal remiges are shorter than more proximal like feathers around the periphery of the bodies, suggesting that

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Received 19 January; accepted 27 May 1998. Acknowledgements. We thank A. Brush, B. Creisler, M. Ellison, W.-D. Heinrich, N. Jacobsen, E. and R. Koppelhus, P. Makovicky, A. Milner, G. Olshevsky, J. Ostrom and H.-P. Schultze for advice, access to 1. Ji, Q. et al. On the sequence and age of the protobird bearing deposits in the Sihetun-Jianshangou area, collections and logistic support; and the National Geographic Society, National Science Foundation Beipao, western Liaoning. Prof. Pap. Strat. Paleo. (in the press). (USA), the American Museum of Natural History, National Natural Science Foundation of China and the 2. Hou, L.-H., Zhou, Z.-H., Martin, L. D. & Feduccia, A. A beaked bird from the Jurassic of China. Ministry of Geology for support. Photographs were taken by O. L. Mazzatenta and K. Aulenback; the Nature 377, 616–618 (1995). latter was also responsible for preliminary preparation of the Caudipteryx specimens. Line drawings are by 40 39 3. Smith, P. E. et al. Dates and rates in ancient lakes: Ar- Ar evidence for an Early Cretaceous age for P.J.C. the Jehol Group, northeast China. Can. J. Earth Sci. 32, 1426–1431 (1995). 4. Smith, J. B., Hailu, Y. & Dodson, P. in The Dinofest Symposium, Abstracts (eds Wolberg, D. L. et al.) 55 Correspondence and requests for materials should be addressed to P.J.C. (e-mail: pcurrie@mcd. (Academy of Natural Sciences, Philadelphia, 1998). gov.ab.ca).